Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Effect of Thyroid Hormone on the Gene Expression of Myostatin in Rat Skeletal Muscle

  • Ma, Yi (Tianjin Institute of Animal Science and Veterinary) ;
  • Chen, Xiaoqiang (Department of Agronomy, Tianjin Agricultural University) ;
  • Li, Qing (State Key Laboratory for Agrobiotechnology, China Agricultural University) ;
  • An, Xiaorong (State Key Laboratory for Agrobiotechnology, China Agricultural University) ;
  • Chen, Yongfu (State Key Laboratory for Agrobiotechnology, China Agricultural University)
  • Received : 2008.05.21
  • Accepted : 2008.09.18
  • Published : 2009.02.01
Download PDF
⟨ Previous Next ⟩

Abstract

Modification of thyroid hormone levels has a profound effect on skeletal muscle differentiation, predominantly through direct regulation involving thyroid hormone receptors. Nevertheless, little is known about the regulation of myostatin gene expression in skeletal muscle due to altered concentrations of thyroid hormone. Thus, the goal of our study was to find out whether altered thyroid states could change the gene expression of myostatin, the most powerful inhibitor of skeletal muscle development. A hyperthyroid state was induced in rats by daily injections of L-thyroxine 20 mg/100 g body weight for 14 days, while a hypothyroid state was induced in another group of rats by administering methimazole (0.04%) in drinking water for 14 days. After a period of 14 days of L-thyroxine treatment we observed a significant increase of myostatin expression both in mRNA and protein level. However, decreased expression of myostatin mRNA and protein were observed in hypothyroid rats. Furthermore, our studies demonstrated that the upregulation of myostatin gene expression might be responsible for the loss of body weight induced by altered thyroid hormone levels. We concluded that myostatin played a role in a metabolic process in muscle that was regulated by thyroid hormone.

Keywords

References

  1. Anderson, J. E., L. Liu and E. Kardami. 1994,The effects of hyperthyroidism on muscular dystrophy in the mdx mouse: greater dystrophy in cardiac and soleus muscle, Muscle Nerve,17:64-73 https://doi.org/10.1002/mus.880170109
  2. Bell, A., A. Gagnon, L. Grunder, S. J. Parikh, T. J. Smith and A. Sorisky. 2000,Functional TSH receptor in human abdominal preadipocytes and orbital fibroblasts, Am. J. Physiol. CellPhysiol. 279:C335-340
  3. Bruno, A. N., D. Pochmann, F. K. Ricachenevsky, C. D. Bonan, M. L. Barreto-Chaves and J. J. Freitas, Sarkis. 2005. 5'- nucleotidase activity is altered by hypo- and hyperthyroidism in platelets from adult rats. Platelets. 16:25-30 https://doi.org/10.1080/0953710042000260164
  4. Carlson, C. J., F. W. Booth and S. E. Gordon. 1999, Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloadin,. Am. J. Physiol. 277:R601-606
  5. Carnac, G., O. Albagli-Curiel, M. Vandromme, C. Pinset, D. Montarras, V. Laudet and A. Bonnieu, 1992. 3,5,3'- Triiodothyronine positively regulates both MyoD1 gene transcription and terminal differentiation in C2 myoblasts, Mo. Endocrinol. 6:1185-1194 https://doi.org/10.1210/me.6.8.1185
  6. Chen, Jian-hai, Wen-juan Wei, Xiao Xiao, Meng-Jin Zhu, Bin Fan and Shu-Hong Zhao. 2008, Expression analysis of miRNAs in porcine fetal skeletal muscle on days 65 and 90 of gestation,Asian-Aust. J. Anim. Sci. 21(7): 954-960
  7. Fazylov, R., E. Soto, S. Cohen and S. Merola. 2008, Laparoscopic Roux-en-Y gastric bypass surgery on morbidly obese patients with hypothyroidism, Obes. Surg. 18(6):644-647 https://doi.org/10.1007/s11695-007-9279-8
  8. Glass, C. K. and J. M. Holloway. 1990, Regulation of gene expression by the thyroid hormone receptor, Biochim. Biophys.Acta. 1032:157-76 https://doi.org/10.1172/JCI114906
  9. Gonzalez-Cadavid, N. F., W. E. Taylor, K. Yarasheski, I. Sinha- Hikim, K. Ma, S. Ezzat, R. Shen, R. Lalani, S. Asa, M. Mamita, G. Nair, S. Arver and S. Bhasin. 1998,Organization of the human myostatin gene and expression in healthy men and HIV-infected men with muscle wasting, Proc. Natl. Acad. Sci. USA. 95:14938-14943 https://doi.org/10.1073/pnas.95.25.14938
  10. Isman, C. A., B. C. Yegen and I. Alican. 2003, Methimazoleinduced hypothyroidism in rats ameliorates oxidative injury in experimental colitis. J. Endocrinol, 177:471-176 https://doi.org/10.1677/joe.0.1770471
  11. Izumo, S., B. Nadal-Ginard and V. Mahdavi. 1986, All members of the MHC multigene family respond to thyroid hormone in a highly tissue-specific manner. Sci. 231:597-600 https://doi.org/10.1126/science.3945800
  12. Jin, Eun-Jung, Inae Kim, C. Young Lee and Byung-Chul Park. 2006, Suppressed cell proliferation and differentiation following an over-expression of myostatin is associated with inhibited expression of insulin-like growth factor II and myogenin in rat L6 myoblasts, Asian-Aust. J. Anim. Sci. 19(10):1508-1513
  13. Joulia, D., H. Bernardi, V. Garandel, F. Rabenoelina, B. Vernus and G. Cabello. 2003, Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin, Exp. Cell Res. 286:263-275 https://doi.org/10.1016/S0014-4827(03)00074-0
  14. Kambadur, R., M. Sharma, T. P. Smith and J. J. Bass. 1997, Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle, Genome. Res. 7:910-916
  15. Kocamis, H., N. Gulmez, S. Aslan and M. Nazli. 2004, Follistatin alters myostatin gene expression in C2C12 muscle cells, Acta.Vet. Hung. 52:135-141 https://doi.org/10.1556/AVet.52.2004.2.1
  16. Kokkinos, A., I. Mourouzis, D. Kyriaki, C. Pantos, N. Katsilambros and D. V. Cokkinos. 2007, Possible implications of leptin, adiponectin and ghrelin in the regulation of energy homeostasis by thyroid hormone, Endocrine, 32(1):30-32 https://doi.org/10.1007/s12020-007-9002-5
  17. Laemmli, U. K. 1970,Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227:680-685 https://doi.org/10.1038/227680a0
  18. Lalani, R., S. Bhasin, F. Byhower, R. Tarnuzzer, M. Grant, R. Shen, S. Asa, S. Ezzat and N. F. Gonzalez-Cadavid. 2000, Myostatin and insulin-like growth factor-I and -II expression in the muscle of rats exposed to the microgravity environment of the NeuroLab space shuttle flight, J. Endocrinol. 167:417-428 https://doi.org/10.1677/joe.0.1670417
  19. Lovejoy, J. C., S. R. Smith, J. J. Zachwieja, G. A. Bray, M. M. Windhauser, P. J. Wickersham, J. D. Veldhuis, R. Tulley and J. A. de, la, Bretonne. 1999, Low-dose T (3) improves the bed rest model of simulated weightlessness in men and women, Am. J. Physiol, 277:E370-379
  20. Ma, K., C. Mallidis, J. Artaza, W. Taylor, N. Gonzalez-Cadavid and S. Bhasin. 2001, Characterization of 5'-regulatory region of human myostatin gene: regulation by dexamethasone in vitro, Am. J. Physiol. Endocrinol. Metab. 281: E1128-1136 https://doi.org/10.1056/NEJMoa040933
  21. McCroskery, S., M. Thomas, L. Maxwell, M. Sharma and R. Kambadur. 2003, Myostatin negatively regulates satellite cell activation and selfrenewal, J. Cell. Biol. 162:1135-1147 https://doi.org/10.1083/jcb.200207056
  22. McPherron, A. C. and S. J. Lee. 1997, Double muscling in cattle due to mutations in the myostatin gene, Proc. Natl. Acad. Sci. USA. 94:12457-12461 https://doi.org/10.1073/pnas.94.23.12457
  23. Monici, M. C., C. Rodolico, A. Toscano, S. Messina, S. Benvenga, C. Messina and G. Vita. 2002, Apoptosis and apoptosis-related proteins in thyroid myopathies, Muscle Nerve. 26:383-388 https://doi.org/10.1002/mus.10212
  24. Nicol, C. J. and D. S. Bruce. 1981, Effect of hyperthyroidism on the contractile and histochemical properties of fast and slow twitch skeletal muscle in the rat, Pflugers. Arch. 390:73-79 https://doi.org/10.1007/BF00582715
  25. Nwokye, L., W. F. Mommaerts, D. R. Simpson, K. Seraydarian and M. Marusich. 1982, Evidence for a direct action of thyroid hormone in specifying muscle properties, Am. J. Physiol. 242: R401-408
  26. Ortiga-Carvalho, T. M., J. Polak, S. McCann and C. C. Pazos- Moura. 1996, Effect of thyroid hormones on pituitary neuromedin B and possible interaction between thyroid hormones and neuromedin B on thyrotropin secretion, Regul. Pept. 67:47-53 https://doi.org/10.1016/S0167-0115(96)00106-1
  27. Rebello, S., E. B. Thompson and A. Gulatin. 1993, Endothelin mechanisms in altered thyroid states in the rat, Eur. J. Pharmacol. 237(1):9-16 https://doi.org/10.1016/0014-2999(93)90086-W
  28. Samuels, H. H., B. M. Forman, Z. D. Horowitz and Z. S. Ye. 1989, Regulation of gene expression by thyroid hormone, Annu. Rev. Physiol. 51:623-639 https://doi.org/10.1146/annurev.ph.51.030189.003203
  29. Scow, R. O. 1951, Effect of growth hormone on muscle and skin collagen in neonatal thyroidectomized rats, Endocrinol. 49:641-646 https://doi.org/10.1210/endo-49-5-641
  30. Scow, R. O. 1953, Effect of growth hormone on various protein fractions in striated muscle of thyroidectomized and hypophysectomized rats, Am. J. Physiol. 173:199-206
  31. Sellitti, D. F., D. Dennison, T. Akamizu, S. Q. Doi, L. D. Kohn and H. Koshiyama. 2000, Thyrotropin regulation of cyclic adenosine monophosphate production in human coronary artery smooth muscle cells, Thyroid. 10:219-225 https://doi.org/10.1089/thy.2000.10.219
  32. Shupnik, M. A., W. W. Chin, J. F. Habener and E. C. Ridgway. 1985, Transcriptional regulation of the thyrotropin subunit genes by thyroid hormone, J. Biol. Chem. 260:2900-2903
  33. Taylor, W. E., S. Bhasin, J. Artaza, F. Byhower, M. Azam, D. H. Willard, Jr., F. C. Kull, Jr. and N. Gonzalez-Cadavid. 2001, Myostatin inhibits cell proliferation and protein synthesis in C2C12 muscle cells, Am. J. Physiol. Endocrinol. Meta. 280:E221-228
  34. Thomas, M., B. Langley, C. Berry, M. Sharma, S. Kirk, J. Bass and R. Kambadur. 2000, Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation, J. Biol. Chem. 275:40235-40243 https://doi.org/10.1074/jbc.M004356200
  35. Urban, F. Jr., G. Cavazos, J. Dunbar, B. Tan, P. Escher, I. S. Tafur and M. Wang. 2000, The important role of residue F268 in ligand binding by LXRbeta, FEBS. Lett. 484:159-163 https://doi.org/10.1016/S0014-5793(00)02130-X
  36. Weaver, J. U. 2008, Classical endocrine diseases causing obesity, Front. Horm. Res. 36:212-228 https://doi.org/10.1159/000115367
  37. Wehling, M., B. Cai and J. G. Tidball. 2000, Modulation of myostatin expression during modified muscle use, FASEB. J. 14:103-110
  38. Weng, Q., E. Saita, G. Watanabe, S. Takahashi, M. Sedqyar, A. K. Suzuki, S. Taneda and K. Taya. 2007, Effect of methimzaoleinduced hypothyroidism on adrenal and gonadal functions in male Japanese quail (Coturnix japonica), J. Reprod. Dev. Dec.53(6):1335-1341 https://doi.org/10.1262/jrd.19081
  39. Zachwieja, J. J., S. R. Smith, I. Sinha-Hikim, N. Gonzalez- Cadavid and S. Bhasin. 1999, Plasma myostatinimmunoreactive protein is increased after prolonged bed rest with low-dose T3 administration, J. Gravit. Physiol. 6:11-15 https://doi.org/10.2174/138920207783591672
  40. Zimmers, T. A., M. V. Davies, L. G. Koniaris, P. Haynes, A. F. Esquela, K. N. Tomkinson, A. C. McPherron, N. M. Wolfman and S. J. Lee. 2002, Induction of cachexia in mice by systemically administered myostatin, Sci. 296:1486-1488 https://doi.org/10.1126/science.1069525

Cited by

  1. Effects of Castration on Androgen Receptor, IGF-I Ea, MGF and Myostatin Gene Expression in Skeletal Muscles of Male Pigs vol.22, pp.8, 2009, https://doi.org/10.5713/ajas.2009.80632
  2. Content of selected amino acids in the gastrocnemius muscle during experimental hypothyroidism in rats vol.60, pp.4, 2009, https://doi.org/10.1515/jvetres-2016-0072